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The gene transformer of anastrepha fruit flies (Diptera, tephritidae) and its evolution in insects.

ABSTRACT: In the tephritids Ceratitis capitata and Bactrocera oleae, the gene transformer acts as the memory device for sex determination, via an auto-regulatory function; and functional Tra protein is produced only in females. This paper investigates the evolution of the gene tra, which was characterised in twelve tephritid species belonging to the less extensively analysed genus Anastrepha. Our study provided the following major conclusions. Firstly, the memory device mechanism used by this gene in sex determination in tephritids likely existed in the common ancestor of the Ceratitis, Bactrocera and Anastrepha phylogenetic lineages. This mechanism would represent the ancestral state with respect to the extant cascade seen in the more evolved Drosophila lineage. Secondly, Transformer2-specific binding intronic splicing silencer sites were found in the splicing regulatory region of transformer but not in doublesex pre-mRNAs in these tephritids. Thus, these sites probably provide the discriminating feature for the putative dual splicing activity of the Tra-Tra2 complex in tephritids. It acts as a splicing activator in dsx pre-mRNA splicing (its binding to the female-specific exon promotes the inclusion of this exon into the mature mRNA), and as a splicing inhibitor in tra pre-mRNA splicing (its binding to the male-specific exons prevents the inclusion of these exons into the mature mRNA). Further, a highly conserved region was found in the specific amino-terminal region of the tephritid Tra protein that might be involved in Tra auto-regulatory function and hence in its repressive splicing behaviour. Finally, the Tra proteins conserved the SR dipeptides, which are essential for Tra functionality.

SUBMITTER: Ruiz MF

PROVIDER: S-EPMC2080774 | biostudies-literature | 2007

REPOSITORIES: biostudies-literature

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The gene transformer of anastrepha fruit flies (Diptera, tephritidae) and its evolution in insects.

Ruiz María Fernanda MF Milano Andreina A Salvemini Marco M Eirín-López José María JM Perondini André L P AL Selivon Denise D Polito Catello C Saccone Giuseppe G Sánchez Lucas L

PloS one 20071128 11

In the tephritids Ceratitis capitata and Bactrocera oleae, the gene transformer acts as the memory device for sex determination, via an auto-regulatory function; and functional Tra protein is produced only in females. This paper investigates the evolution of the gene tra, which was characterised in twelve tephritid species belonging to the less extensively analysed genus Anastrepha. Our study provided the following major conclusions. Firstly, the memory device mechanism used by this gene in sex ...[more]

PMID: 18043746

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Project description:BackgroundIn the tephritids Ceratitis, Bactrocera and Anastrepha, the gene transformer provides the memory device for sex determination via its auto-regulation; only in females is functional Tra protein produced. To date, the isolation and characterisation of the gene transformer-2 in the tephritids has only been undertaken in Ceratitis, and it has been shown that its function is required for the female-specific splicing of doublesex and transformer pre-mRNA. It therefore participates in transformer auto-regulatory function. In this work, the characterisation of this gene in eleven tephritid species belonging to the less extensively analysed genus Anastrepha was undertaken in order to throw light on the evolution of transformer-2.ResultsThe gene transformer-2 produces a protein of 249 amino acids in both sexes, which shows the features of the SR protein family. No significant partially spliced mRNA isoform specific to the male germ line was detected, unlike in Drosophila. It is transcribed in both sexes during development and in adult life, in both the soma and germ line. The injection of Anastrepha transformer-2 dsRNA into Anastrepha embryos caused a change in the splicing pattern of the endogenous transformer and doublesex pre-mRNA of XX females from the female to the male mode. Consequently, these XX females were transformed into pseudomales. The comparison of the eleven Anastrepha Transformer-2 proteins among themselves, and with the Transformer-2 proteins of other insects, suggests the existence of negative selection acting at the protein level to maintain Transformer-2 structural features.ConclusionsThese results indicate that transformer-2 is required for sex determination in Anastrepha through its participation in the female-specific splicing of transformer and doublesex pre-mRNAs. It is therefore needed for the auto-regulation of the gene transformer. Thus, the transformer/transfomer-2 > doublesex elements at the bottom of the cascade, and their relationships, probably represent the ancestral state (which still exists in the Tephritidae, Calliphoridae and Muscidae lineages) of the extant cascade found in the Drosophilidae lineage (in which tra is just another component of the sex determination gene cascade regulated by Sex-lethal). In the phylogenetic lineage that gave rise to the drosophilids, evolution co-opted for Sex-lethal, modified it, and converted it into the key gene controlling sex determination.

Project description:Odorant-binding proteins (OBPs) are of great importance for survival and reproduction since they participate in initial steps of the olfactory signal transduction cascade, solubilizing and transporting chemical signals to the olfactory receptors. A comparative analysis of OBPs between closely related species may help explain how these genes evolve and are maintained under natural selection and how differences in these proteins can affect olfactory responses. We studied OBP genes in the closely related species Anastrepha fraterculus and A. obliqua, which have different host preferences, using data from RNA-seq cDNA libraries of head and reproductive tissues from male and female adults, aiming to understand the speciation process occurred between them.We identified 23 different OBP sequences from Anastrepha fraterculus and 24 from A. obliqua, which correspond to 20 Drosophila melanogaster OBP genes. Phylogenetic analysis separated Anastrepha OBPs sequences in four branches that represent four subfamilies: classic, minus-C, plus-C and dimer. Both species showed five plus-C members, which is the biggest number found in tephritids until now. We found evidence of positive selection in four genes and at least one duplication event that preceded the speciation of these two species. Inferences on tertiary structures of putative proteins from these genes revealed that at least one positively selected change involves the binding cavity (the odorant binding region) in the plus-C OBP50a.A. fraterculus and A. obliqua have a bigger OBP repertoire than the other tephritids studied, though the total number of Anastrepha OBPs may be larger, since we studied only a limited number of tissues. The contrast of these closely related species reveals that there are several amino acid changes between the homologous genes, which might be related to their host preferences. The plus-C OBP that has one amino acid under positive selection located in the binding cavity may be under a selection pressure to recognize and bind a new odorant. The other positively selected sites found may be involved in important structural and functional changes, especially ones in which site-specific changes would radically change amino acid properties.

Dataset Information

The gene transformer of anastrepha fruit flies (Diptera, tephritidae) and its evolution in insects.

Publications

The gene transformer of anastrepha fruit flies (Diptera, tephritidae) and its evolution in insects.

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